Defence-related priming and responses to recurring drought: Two manifestations of plant transcriptional memory mediated by the ABA and JA signalling pathways.

Collective evidence from agricultural practices and from scientific research has demonstrated that plants can alter their phenotypic responses to repeated biotic and abiotic stresses or their elicitors. A coordinated reaction at the organismal, cellular, and genome levels has suggested that plants can "remember" an earlier stress and modify their future responses, accordingly. Stress memory may increase a plant's survival chances by improving its tolerance/avoidance abilities and may provide a mechanism for acclimation and adaptation.

Dehydration Stress Memory: Gene Networks Linked to Physiological Responses During Repeated Stresses of .

Stress memory refers to the observation that an initial, sub-lethal stress alters plants' responses to subsequent stresses. Previous transcriptome analyses of maize seedlings exposed to a repeated dehydration stress has revealed the existence of transcriptional stress memory in . Whether drought-related physiological responses also display memory and how transcriptional memory translates into physiological memory are fundamental questions that are still unanswered.

Myotubularins, PtdIns5P, and ROS in ABA-mediated stomatal movements in dehydrated Arabidopsis seedlings.

Myotubularins (MTMs) are lipid phosphoinositide 3-phosphate phosphatases and the product of their enzyme activity - phosphoinositide 5-phosphate (PtdIns5P) - functions as a signalling molecule in pathways involved in membrane dynamics and cell signalling. Two Arabidopsis genes, AtMTM1 and AtMTM2, encode enzymatically active phosphatases but although AtMTM1 deficiency results in increased tolerance to dehydration stress and a decrease in cellular PtdIns5P, the role of AtMTM2 is less clear, as it does not contribute to the PtdIns5P pool upon dehydration stress. Here we analysed the involvement of AtMTM1, AtMTM2 and PtdIns5P in the response of Arabidopsis seedlings to dehydration stress/ABA, and found that both AtMTM1 and AtMTM2 were involved but affected oppositely stomata movement and the accumulation of reactive oxygen species (ROS, e.

The jasmonic acid-signalling and abscisic acid-signalling pathways cross talk during one, but not repeated, dehydration stress: a non-specific 'panicky' or a meaningful response?

Experiencing diverse and recurring biotic and abiotic stresses throughout life, plants have evolved mechanisms to respond, survive and, eventually, adapt to changing habitats. The initial response to drought involves a large number of genes that are involved also in response to other stresses. According to current models, this initial response is non-specific, becoming stress-specific only at later time points.

Memory responses of jasmonic acid-associated Arabidopsis genes to a repeated dehydration stress.

Dehydration stress activates numerous genes co-regulated by diverse signaling pathways. Upon repeated exposures, however, a subset of these genes does not respond maintaining instead transcription at their initial pre-stressed levels ('revised-response' genes). Most of these genes are involved in jasmonic acid (JA) biosynthesis, JA-signaling and JA-mediated stress responses.

Subcellular localizations of Arabidopsis myotubularins MTM1 and MTM2 suggest possible functions in vesicular trafficking between ER and cis-Golgi.

The two Arabidopsis genes AtMTM1 and AtMTM2 encode highly similar phosphoinositide 3-phosphatases from the myotubularin family. Despite the high-level conservation of structure and biochemical activities, their physiological roles have significantly diverged. The nature of a membrane and the concentrations of their membrane-anchored substrates (PtdIns3P or PtdIns3,5P2) and/or products (PtdIns5P and PtdIns) are considered critical for determining the functional specificity of myotubularins.

Molecular mechanism of the priming by jasmonic acid of specific dehydration stress response genes in Arabidopsis.

Background: Plant genes that provide a different response to a similar dehydration stress illustrate the concept of transcriptional 'dehydration stress memory'. Pre-exposing a plant to a biotic stress or a stress-signaling hormone may increase transcription from response genes in a future stress, a phenomenon known as 'gene priming'. Although known that primed transcription is preceded by accumulation of H3K4me3 marks at primed genes, what mechanism provides for their appearance before the transcription was unclear.

Transcriptional 'memory' of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes.

Drought, salinity, extreme temperature variations, pathogen and herbivory attacks are recurring environmental stresses experienced by plants throughout their life. To survive repeated stresses, plants provide responses that may be different from their response during the first encounter with the stress. A different response to a similar stress represents the concept of 'stress memory'.

Endogenous ABA Extraction and Measurement from Leaves.

The endogenous messenger, the phytohormone abscisic acid (ABA) plays a major role in plant's adaption to drought, salinity, cold and other abiotic stresses. In addition to abiotic stress signaling, ABA is involved also in developmental regulation and in responses to diverse biotic stresses. Dehydration stress results in a strong increase in endogenous ABA levels, which can be perceived by RCAR/PYR1/PYL receptors, initiating the ABA signaling pathway to coordinate the genome-wide gene expression, and plants adaptive physiological responses.

ATX1/AtCOMPASS and the H3K4me3 marks: how do they activate Arabidopsis genes?

Despite the proven correlation between gene transcriptional activity and the levels of tri-methyl marks on histone 3 lysine4 (H3K4me3) of their nucleosomes, whether H3K4me3 contributes to, or 'registers', activated transcription is still controversial. Other questions of broad relevance are whether histone-modifying proteins are involved in the recruitment of Pol II and the general transcription machinery and whether they have roles other than their enzyme activities. We address these questions as well as the roles of the ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1), of the COMPASS-related (AtCOMPASS) protein complex, and of their product, H3K4me3, at ATX1-dependent genes.

Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana.

Background: Pre-exposing plants to diverse abiotic stresses may alter their physiological and transcriptional responses to a subsequent stress, suggesting a form of "stress memory". Arabidopsis thaliana plants that have experienced multiple exposures to dehydration stress display transcriptional behavior suggesting "memory" from an earlier stress. Genes that respond to a first stress by up-regulating or down-regulating their transcription but in a subsequent stress provide a significantly different response define the 'memory genes' category.

ABA signaling is necessary but not sufficient for RD29B transcriptional memory during successive dehydration stresses in Arabidopsis thaliana.

Plants subjected to a prior dehydration stress were seen to have altered transcriptional responses during a subsequent dehydration stress for up to 5 days after the initial stress. The abscisic acid (ABA) inducible RD29B gene of Arabidopsis thaliana was strongly induced after the first stress and displayed transcriptional memory with transcript levels nine-fold higher during the second dehydration stress. These increased transcript levels were due to an increased rate of transcription and are associated with an altered chromatin template during the recovery interval between the dehydration stresses.

Different gene-specific mechanisms determine the 'revised-response' memory transcription patterns of a subset of A. thaliana dehydration stress responding genes.

Plants that have experienced several exposures to dehydration stress show increased resistance to future exposures by producing faster and/or stronger reactions, while many dehydration stress responding genes in Arabidopsis thaliana super-induce their transcription as a 'memory' from the previous encounter. A previously unknown, rather unusual, memory response pattern is displayed by a subset of the dehydration stress response genes. Despite robustly responding to a first stress, these genes return to their initial, pre-stressed, transcript levels during the watered recovery; surprisingly, they do not respond further to subsequent stresses of similar magnitude and duration.

H3K27me3 and H3K4me3 chromatin environment at super-induced dehydration stress memory genes of Arabidopsis thaliana.

Pre-exposure to a stress may alter the plant's cellular, biochemical, and/or transcriptional responses during future encounters as a 'memory' from the previous stress. Genes increasing transcription in response to a first dehydration stress, but producing much higher transcript levels in a subsequent stress, represent the super-induced 'transcription memory' genes in Arabidopsis thaliana. The chromatin environment (histone H3 tri-methylations of Lys 4 and Lys 27, H3K4me3, and H3K27me3) studied at five dehydration stress memory genes revealed existence of distinct memory-response subclasses that responded differently to CLF deficiency and displayed different transcriptional activities during the watered recovery periods.

Four distinct types of dehydration stress memory genes in Arabidopsis thaliana.

Background: How plants respond to dehydration stress has been extensively researched. However, how plants respond to multiple consecutive stresses is virtually unknown. Pre-exposure to various abiotic stresses (including dehydration) may alter plants' subsequent responses by improving resistance to future exposures.

ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes.

Tri-methylated H3 lysine 4 (H3K4me3) is associated with transcriptionally active genes, but its function in the transcription process is still unclear. Point mutations in the catalytic domain of ATX1 (ARABIDOPSIS TRITHORAX1), a H3K4 methyltransferase, and RNAi knockdowns of subunits of the AtCOMPASS-like (Arabidopsis Complex Proteins Associated with Set) were used to address this question. We demonstrate that both ATX1 and AtCOMPASS-like are required for high level accumulation of TBP (TATA-binding protein) and Pol II at promoters and that this requirement is independent of the catalytic histone modifying activity.

Evolution of the PWWP-domain encoding genes in the plant and animal lineages.

Background: Conserved domains are recognized as the building blocks of eukaryotic proteins. Domains showing a tendency to occur in diverse combinations ('promiscuous' domains) are involved in versatile architectures in proteins with different functions. Current models, based on global-level analyses of domain combinations in multiple genomes, have suggested that the propensity of some domains to associate with other domains in high-level architectures increases with organismal complexity.

Multiple exposures to drought 'train' transcriptional responses in Arabidopsis.

Pre-exposure to stress may alter plants' subsequent responses by producing faster and/or stronger reactions implying that plants exercise a form of 'stress memory'. The mechanisms of plants' stress memory responses are poorly understood leaving this fundamental biological question unanswered. Here we show that during recurring dehydration stresses Arabidopsis plants display transcriptional stress memory demonstrated by an increase in the rate of transcription and elevated transcript levels of a subset of the stress-response genes (trainable genes).

Divergent functions of the myotubularin (MTM) homologs AtMTM1 and AtMTM2 in Arabidopsis thaliana: evolution of the plant MTM family.

Myotubularin and myotubularin-related proteins are evolutionarily conserved in eukaryotes. Defects in their function result in muscular dystrophy, neuronal diseases and leukemia in humans. In contrast to the animal lineage, where genes encoding both active and inactive myotubularins (phosphoinositide 3-phosphatases) have appeared and proliferated in the basal metazoan group, myotubularin genes are not found in the unicellular relatives of green plants.

Viscoelastic properties of cell walls of single living plant cells determined by dynamic nanoindentation.

Plant development results from controlled cell divisions, structural modifications, and reorganizations of the cell wall. Thereby, regulation of cell wall behaviour takes place at multiple length scales involving compositional and architectural aspects in addition to various developmental and/or environmental factors. The physical properties of the primary wall are largely determined by the nature of the complex polymer network, which exhibits time-dependent behaviour representative of viscoelastic materials.

The Arabidopsis trithorax-like factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways.

Emerging evidence suggests that the molecular mechanisms driving the responses of plants to environmental stresses are associated with specific chromatin modifications. Here, we demonstrate that the Arabidopsis trithorax-like factor ATX1, which trimethylates histone H3 at lysine 4 (H3K4me3), is involved in dehydration stress signaling in both abscisic acid (ABA)-dependent and ABA-independent pathways. The loss of function of ATX1 results in decreased germination rates, larger stomatal apertures, more rapid transpiration and decreased tolerance to dehydration stress in atx1 plants.

Two distinct roles of ARABIDOPSIS HOMOLOG OF TRITHORAX1 (ATX1) at promoters and within transcribed regions of ATX1-regulated genes.

The Arabidopsis thaliana trithorax-like protein, ATX1, shares common structural domains, has similar histone methyltransferase (HMT) activity, and belongs in the same phylogenetic subgroup as its animal counterparts. Most of our knowledge of the role of HMTs in trimethylating lysine 4 of histone H3 (H3K4me3) in transcriptional regulation comes from studies of yeast and mammalian homologs. Little is known about the mechanism by which ATX1, or any other HMT of plant origin, affects transcription.

A cytoplasm-specific activity encoded by the Trithorax-like ATX1 gene.

Eukaryotes produce multiple products from a single gene locus by alternative splicing, translation or promoter usage as mechanisms expanding the complexity of their proteome. Trithorax proteins, including the Arabidopsis Trithorax-like protein ATX1, are histone modifiers regulating gene activity. Here, we report that a novel member of the Trithorax family has a role unrelated to chromatin.